Effects of Crude Oil on Survival and Development in Embryonated Eggs in Callinectes Sapidus Rathbun, 1896 (Decapoda, Portunidae)
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Effects of crude oil on survival and development in embryonated eggs in Callinectes sapidus Rathbun, 1896 (Decapoda, Portunidae) Kelsie L. Kelly1 and Caz M. Taylor2 1 Brooklyn Law School, Brooklyn, NY, USA 2 Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA, USA ABSTRACT Blue crabs, Callinectes sapidus Rathbun, 1896, are ubiquitous along the Atlantic and Gulf coasts of the USA. These organisms play an integral role in the ecosystems of the Gulf of Mexico (GOM), where not only are they a keystone species, but are also socioeconomically important. The survival of embryonated eggs is necessary to ensure adequate recruitment into the next generation. Because the 2010 Deepwater Horizon oil spill (DWH) occurred during the peak of the blue crab spawning season, the incident likely impacted blue crab embryos. In order to assess the effect of oil on embryonic growth and development, we collected embryonated eggs from seven different female blue crabs from the GOM throughout the spawning season and exposed them to an oil concentration of 500 ppb (the approximate concentration of oil at the surface water near the site of the Deepwater Horizon oil rig). Exposure to oil at this concentration caused a significantly larger proportion of prezoeae vs. zoeae to hatch from embryonated eggs in experiments lasting longer than 4 days. Exposure to oil did not significantly affect overall survival or development rate. The prezoeal stage is a little-studied stage of blue crab development. Though it may or may not be a normal stage of development, this stage has been found to occur in suboptimal conditions and has lower survival than zoeal stages. The larger proportion of prezoeae following prolonged exposure to oil thus indicates 7 March 2017 Submitted that crude oil at concentrations likely to be experienced by crabs after the DWH Accepted 22 October 2018 Published 11 December 2018 spill negatively impacted the development of blue crab embryos. In addition to Corresponding author providing insight into the effects of the DWH, this study sheds light on Kelsie L. Kelly, [email protected] embryonic development in blue crabs, a critical, but poorly investigated phase of ’ Academic editor this important species life cycle. Suchana Chavanich Additional Information and Subjects Developmental Biology, Marine Biology, Toxicology, Ecotoxicology, Environmental Declarations can be found on Impacts page 9 Keywords Blue crab, Callinectes sapidus, Deepwater horizon, Oil spill, Blue crab development, DOI 10.7717/peerj.5985 Invertebrate embryos, Oil exposure, Prezoea Copyright 2018 Kelly and Taylor INTRODUCTION Distributed under Creative Commons CC-BY 4.0 Marine organisms may be most vulnerable to the effects of toxicants at the embryonic stage due to the intense period of cellular activity that occurs during development How to cite this article Kelly KL, Taylor CM. 2018. Effects of crude oil on survival and development in embryonated eggs in Callinectes sapidus Rathbun, 1896 (Decapoda, Portunidae). PeerJ 6:e5985 DOI 10.7717/peerj.5985 (Connor, 1972; Lee et al., 1999). Studies examining the effects of various pollutants found detrimental effects on the growth and development of marine organisms (Lee & Oshima, 1998; Klumpp et al., 2002; Bellas et al., 2008). One pollutant to which marine organisms are likely to be exposed is crude oil released from natural seeps but also from oil spills, such as the Exxon Valdez spill in 1989 and the more recent Deepwater Horizon oil spill (DWH) in 2010. The DWH was the largest oil spill in US history and released approximately 4.1 million barrels of oil into the northern Gulf of Mexico (NGOM) from 20 April 2010 to 15 July 2010 (McNutt et al., 2012; Allan, Smith & Anderson, 2012). During the spill, oil concentrations in the surface waters were found to be as high as 500 ppb (Chiasson & Taylor, 2017; Wade et al., 2011). Previous research has shown that oil at concentrations as low as 0.4 ppb has significant impacts on the growth and development of herring embryos (Clupea pallasi)(Carls, Rice & Hose, 1999). Salmon embryos (Oncorhynchus gorbuscha) exposed to oil from the Exxon Valdez spill incurred genetic damage, which could be passed on to future offspring (Bue, Sharr & Seeb, 1998; Heintz et al., 2000). Heintz et al. (2000) found that polycyclic aromatic hydrocarbons, a class of over 100 compounds found in crude oil, at concentrations of 5.4 ppb resulted in a 15% decrease in juvenile survival. Sea urchin embryos (Strongylocentrotus purpuratus) that were exposed to crude oil experienced developmental delays, slower growth rate, abnormal cleavage and increased mortality (Allen, 1971). One organism that may have been exposed to oil released from the DWH spill was the blue crab, Callinectes sapidus Rathbun, 1896. Blue crabs are highly abundant in the NGOM and are found in their juvenile and adult stages in near-shore estuarine benthic habitats (Guillory, Perry & VanderKooy, 2001). In the spring and summer, female blue crabs migrate offshore to spawn, often to barrier islands or sand shoals (Gelpi et al., 2009). The DWH overlapped with blue crab spawning in both timing and location (Gelpi et al., 2009; Grey et al., 2015). Female blue crabs carry eggs on their abdomen in a mass known as a ‘sponge’, and due to the primarily benthic lifestyle of blue crabs, prolonged exposure of the sponge to oiled sediments is likely (Burns & Teal, 1979; Hines, Lipcius & Haddon, 1987). In addition to exposure occurring in the year of the spill, exposure could occur for many years afterwards due to the persistence of elevated concentrations of oil within the sediments for up to 10 years (Burns & Teal, 1979). It is important to understand the effect of oil on blue crabs due to the ecological and economic significance of this species within the Gulf of Mexico (GOM; Darnell et al., 2009; Gelpi et al., 2009; Alloy et al., 2015; Grey et al., 2015). Studies evaluating the effects of oil on blue crabs have focused on the larval and especially postlarval stages. Such studies have shown some sublethal effects, but have not demonstrated an increase in mortality or any reduction in population size as a result of exposure (Lee, Ryan & Neuhauser, 1976; Pearson et al., 1981; Wang & Stickle, 1988; Alloy et al., 2015; Giltz & Taylor, 2017; Chiasson & Taylor, 2017). However, because eggs may suffer prolonged exposure and because embryonic stages may be particularly vulnerable, it is necessary that we evaluate the effects of oil at the embryonic stage in order to investigate the potential damage caused by oil to the GOM blue crab population. Kelly and Taylor (2018), PeerJ, DOI 10.7717/peerj.5985 2/12 Figure 1 Developmental stages of embryonated eggs in Callinectes sapidus Embryonic stages of Callinectes sapidus Rathbun, 1896. (A) Stage 3 embryonated eggs are approximately ¾ yolk, (b) Stage 4 embryonated eggs are approximately ½ yolk, (C) Stage 5 embryonated eggs are approximately ¼ yolk, (D) Stage 6 embryonated eggs display faint eye spots, (E) Stage 7 embryonated eggs display faint abdominal lines, (F) Stage 8 embryonated eggs display darker and more defined abdominal lines, mouth parts are visible, and eyes are teardrop shaped, (G) Stage 9 embryonated eggs have distinct chromato- phores, eyes are elliptical and dark, and heart beat is apparent in living specimens, (H) Larval prezoea, (I) Larval zoea. Average diameter for embryonated eggs is approximately 267 mm and average larval carapace width is approximately 278 mm(Darnell et al., 2009). Photographs by Kelsie Kelly. Full-size DOI: 10.7717/peerj.5985/fig-1 Blue crab embryos undergo nine stages of development before hatching into a free-swimming larva known as a zoea (Fig. 1; DeVries, Epifanio & Dittel, 1983). Some researchers have noted an additional stage that seems to occur between the ninth embryonic stage and the zoeal stages known as a ‘prezoea’ (Robertson, 1938; Churchill, 1942). In the prezoeal stage, setae and spines are invaginated and the body is covered in a cuticle from which it must break free (Davis, 1965). There is some controversy as to whether the prezoeal stage is a natural, but brief, stage of development vs. an abnormality caused by poor environmental conditions (Sandoz & Rogers, 1944; Van Engel, 1958; Clark, Calazans & Pohle, 1998). Prezoeae are highly vulnerable due to a decreased Kelly and Taylor (2018), PeerJ, DOI 10.7717/peerj.5985 3/12 swimming ability and have a reduced rate of survival such that a prolongation of this stage would have a negative impact on the organism (Clark, Calazans & Pohle, 1998). In this study, we compared the development rates, survival and the stage upon hatching of embryonated blue crab eggs exposed to the concentration of oil at the site of the DWH to unexposed (control) embryonated eggs, in order to assess the effects of the crude oil on embryonic development. MATERIALS AND METHODS We conducted an oil exposure experiment seven times on eggs collected from seven different female blue crabs. Egg masses were obtained from females, with permission from the Mississippi Department of Marine Resources, and were assigned an identification number 1–7 based on date caught. The crabs were collected via crab pots from within the Mississippi Sound (collection dates and locations for the seven egg masses were #1: 6 June 2015, 3020′42″N8834′42″W; #2 and #3: 27 June 2015, 3017′10″N8835′25″W; #4 and #5: 8 July 2015, 3018′47″N8919′16″W; #6 and #7: 22 July 2015 3018′47″N8917′ 68″W). For each experiment, the egg mass was removed from the female and the female was subsequently released. The egg mass was transported approximately one and a half hours away to Tulane University, New Orleans. As described by Lee et al. (1999), pieces of the egg mass were then placed in a container of seawater and shaken gently in order to dislodge the individual eggs from the egg mass.